In 1850, Miller moved to Keokuk, Iowa, which was a state more amenable to his views on slavery, and he immediately freed his few slaves who had come with his family from Kentucky. Active in Iowa politics, he supported Abraham Lincoln in the 1860 election. Lincoln nominated Miller to the Supreme Court on July 16, 1862, after the beginning of the American Civil War. His reputation was so high that Miller was confirmed half an hour after the Senate received notice of his nomination.

He later joined the majority opinions in United States v. Cruikshank and the Civil Rights Cases, holding that the amendment did not give the U.S. government the power to stop private—as opposed to state-sponsored—discrimination against blacks. In Ex Parte Yarbrough, 110 U.S. 651 (1884), however, Miller held that the federal government had broad authority to act to protect black voters from violence by the Ku Klux Klan and other private groups. Miller also supported the use of broad federal power under the Commerce Clause to override state regulations, as in Wabash v. Illinois.

Justice Miller wrote more opinions than any other Supreme Court Justice,[1] leading future Chief JusticeWilliam Rehnquist to describe him as "very likely the dominant figure" on the Court in his time.[2] When Chief Justice Salmon P. Chase died in 1873, attorneys and law journals across the country lobbied for Miller to be appointed to succeed him, but President Ulysses Grant was determined to appoint an outsider; he ultimately chose Morrison Waite.

In the winter of 1889 and spring of 1890, Justice Miller delivered a series of ten lectures on constitutional law at the National University School of Law in Washington D.C. They were published posthumously, along with two earlier lectures delivered in 1887.[3]

Miller, a religious liberal, belonged to the Unitarian Church and served as President of the Unitarians' National Conference. He died in Washington, D.C., while still a member of the Court. Following his death in 1890, his funeral was held at Keokuk's First Unitarian Church;[4] Miller had been one of the congregation's founders.[5] He is buried at Oakland Cemetery in Keokuk, Iowa.

Miller’s first wife was Lucy Love Ballinger Miller (1827 – 1854) whom he married in 1842, and with whom he had three daughters. In 1856, he married Eliza Winter Reeves (1827 – 1900), with whom he had a son and daughter.[5] The second of his five children, Patty Miller Stocking, as an adult wrote and published letters on European travel.

^Green, Michael. “Justice of Shattered Dreams (book review)”, H-Net (2006). Justice Miller wrote 616 opinions in his 28 years on the Court; Justice Field (whose 34 year SCOTUS tenure mostly overlapped Miller's) wrote 544 opinions; Chief Justice Marshall wrote 508 opinions in his 33 years on the Court.